AbstractAn open and dry vegetation belt separates Amazonia (AM) and the Atlantic Forest (AF). Evidence from palaeoclimatic and phylogenetic studies suggests past connections between these forests during cycles of increased humidity through the formation of forest corridors. The distinctive northern AF avifauna is known to have affinities both with AM and the southern AF. Still, the extent of how these two regions contributed to the assemblage of this avifauna remains poorly understood. Using historical demographic analyses and comparative phylogeography based on sub‐genomic genetic sampling, we assessed how past connections between AM and AF led to shared vicariance and colonization events in four avian AF endemic taxa. Our results supported the occurrence of humid forest corridors promoting the contact between AF and AM populations and suggested two vicariant events and two colonization events from AF to AM. Population divergences were mostly non‐synchronous and occurred multiple times during the Pleistocene. Historical gene flow was prevalent across study groups, supporting migration flows after the initial separation between AM and AF – a pattern previously unknown in birds between these regions. Idiosyncratic histories and divergent demographic syndromes suggest that organisms' responses to climate‐driven habitat shifts broadly depend on their ecological attributes. This study strengthened our knowledge of past connections between AM and AF and provided demographic scenarios amenable for testing in other groups of co‐distributed organisms.